Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI

Abstract

The present report reviews a series of functional magnetic resonance imaging (fMRI) activation studies conducted in parallel in awake monkeys and humans using the same motion stimuli in both species. These studies reveal that motion stimuli engage largely similar cortical regions in the two species. These common regions include MT/V5 and its satellites, of which FST contributes more to the human motion complex than is generally assumed in human imaging. These results also establish a direct link between selectivity of MT/V5 neurons for speed gradients and functional activation of human MT/V5 by three-dimensional (3D) structure from motion stimuli. On the other hand, striking functional differences also emerged: in humans V3A and several regions in the intraparietal sulcus (IPS) are much more motion sensitive than their simian counterparts.

Introduction

Motion has attracted a lot of interest in psychology and also neuroscience, as witnessed by the present special issue. One reason is that motion processing has many behavioral functions (Nakayama, 1985). Motion processing gives rise to perception of object motion and of self-motion. It is also used to control eye movements, pursuit and optokinetic nystagmus, as well as to guide movements of body parts and locomotion. Finally, it gives rise to the perception of two-dimensional (2D) shape (kinetic boundaries) and allows the extraction of three-dimensional (3D) structure (the kinetic depth effect and motion parallax). A second important reason for the continuing interest in motion processes is that direction selective cells have been identified as potential neural substrates of motion processing in striate cortex (Hubel & Wiesel, 1962) and extrastriate cortex (Allman and Kaas, 1971, Dubner and Zeki, 1971).

When attempting to relate human perception to single neurons recorded in the wake macaque one faces two important issues. The first concerns the part of the monkey brain where single neurons should be recorded from. For motion processing the standard answer has been MT/V5 (Britten, Shadlen, Newsome, & Movshon, 1992), because almost all MT/V5 neurons are direction selective (Albright, 1984; Dubner and Zeki, 1971, Lagae et al., 1994). Other regions also contain sizeable proportions of direction selective neurons and have received less attention (see Celebrini & Newsome, 1994). The second question relates to the homology between cortical areas explored with single-cell recording in the monkey and cortical regions in the human brain. Functional imaging, positron emission tomography (PET) and more recently, functional magnetic resonance imaging (fMRI) may help solve these two issues. Indeed, functional imaging reveals the overall pattern of regions involved in behavioral functions. In fact, fMRI and single-cell studies complement each other by operating at different levels of integration (Churchland & Sejnowski, 1988). The microelectrode provides a detailed account of the properties of single neurons, whereas the fMRI signals presumably reflect the pooled activity of large populations of neurons. Hence, most recent imaging studies in humans try to relate their findings to single-cell properties. For example, when we reported that several regions in the human brain in addition to hMT/V5+ were sensitive to motion (Dupont, Orban, De Bruyn, Verbruggen, & Mortelmans, 1994), we related this finding to the many monkey cortical areas which contain sizable proportions of direction selective neurons. This assumes, however, that there is a one-to-one relationship between the different monkey cortical areas, e.g. the 30 or so extrastriate areas, and their human counterparts.

We know that a complete homology between cortical areas of humans and monkeys is highly unlikely, given the anatomical and behavioral differences between the two species, and the 30 million years that separate the emergence of the two species during evolution. Until recently, we had no technique to identify those cortical areas where the homology holds up and those where it does not. fMRI in the awake monkey holds the potential to resolve this issue and provides the missing link between human functional imaging and monkey single-cell recording. Although several groups have reported imaging in awake monkeys (Dubowitz et al., 1998; Logothetis, Guggenberger, Peled, & Pauls, 1999; Stefanacci et al., 1998), systematic studies have appeared only recently (Leite et al., 2002; Nakahara, Hayashi, Konishi, & Miyashita, 2002; Vanduffel et al., 2001, Vanduffel et al., 2002). The more recent ones (Nakahara et al., 2002, Vanduffel et al., 2002) have also explicitly compared functional maps in human and non-human primates. This interspecies comparison for cortical regions involved in motion processing is the topic of the present report. It includes two sets of studies: those using simple random dot translation and those related to the extraction of 3D structure from motion. The latter draws on the material reported in Vanduffel et al. (2002), and to a lesser degree on the preceding human study (Orban, Sunaert, Todd, van Hecke, & Marchal, 1999). The translation part combines the two reports that dealt with human and monkey fMRI separately: Sunaert, van Hecke, Marchal, & Orban (1999) and Vanduffel et al. (2001), respectively. Initially, Vanduffel et al. (2001) emphasized the similarity between the activation pattern in the two species, with the exception of V3A. Yet, further experiments and the insight from the 3D structure from motion study have made it clear that the cortical networks processing translation stimuli include regions that are similar in the two species and others that are dissimilar. The part of the visual system that differs between humans and monkeys for both types of stimuli includes not only V3A, but also, and perhaps even more prominently, the intraparietal sulcus (IPS).